Abstract

Fiber-reinforced hydrogels are a class of soft composite materials that have seen increased use across a wide variety of biomedical applications. However, existing fabrication techniques for these hydrogels are unable to realize biologically relevant macro/mesoscale geometries. To address this limitation, this paper presents a novel air-assisted, dual-polarity electrospinning printhead that converges high-strength electric fields, with low velocity air flow to remove the collector dependency seen with traditional far-field electrospinning setups. The use of this printhead in conjunction with different configurations of deformable collection templates has resulted in the production of three classes of fiber-reinforced hydrogel prototype geometries, viz., (i) tubular geometries with bifurcations and mesoscale texturing; (ii) hollow, nontubular geometries with single and dual-entrances; and (iii) three-dimensional (3D) printed flat geometries with varying fiber density. All three classes of prototype geometries were mechanically characterized to have properties that were in line with those observed in living soft tissues. With the realization of this printhead, biologically relevant macro/mesoscale geometries can be realized using fiber-reinforced hydrogels to aid a wide array of biomedical applications.

References

1.
Butcher
,
A. L.
,
Offeddu
,
G. S.
, and
Oyen
,
M. L.
,
2014
, “
Nanofibrous Hydrogel Composites as Mechanically Robust Tissue Engineering Scaffolds
,”
Trends Biotechnol.
,
32
(
11
), pp.
564
570
.10.1016/j.tibtech.2014.09.001
2.
Shapiro
,
J. M.
, and
Oyen
,
M. L.
,
2013
, “
Hydrogel Composite Materials for Tissue Engineering Scaffolds
,”
JOM
,
65
(
4
), pp.
505
516
.10.1007/s11837-013-0575-6
3.
Tonsomboon
,
K.
,
Butcher
,
A. L.
, and
Oyen
,
M. L.
,
2017
, “
Strong and Tough Nanofibrous Hydrogel Composites Based on Biomimetic Principles
,”
Mater. Sci. Eng. C
,
72
, pp.
220
227
.10.1016/j.msec.2016.11.025
4.
Tonsomboon
,
K.
, and
Oyen
,
M. L.
,
2013
, “
Composite Electrospun Gelatin Fiber-Alginate Gel Scaffolds for Mechanically Robust Tissue Engineered Cornea
,”
J. Mech. Behav. Biomed. Mater
,
21
, pp.
185
194
.10.1016/j.jmbbm.2013.03.001
5.
Strange
,
D. G. T.
,
Tonsomboon
,
K.
, and
Oyen
,
M. L.
,
2014
, “
Mechanical Behaviour of Electrospun Fibre-Reinforced Hydrogels
,”
J. Mater. Sci. Mater. Med.
,
25
(
3
), pp.
681
690
.10.1007/s10856-013-5123-y
6.
Williams
,
A.
,
Nowak
,
J. F.
,
Dass
,
R.
,
Samuel
,
J.
, and
Mills
,
K. L.
,
2018
, “
Toward Morphologically Relevant Extracellular Matrix In Vitro Models: 3D Fiber Reinforced Hydrogels
,”
Front. Physiol.
,
9
, p.
966
.10.3389/fphys.2018.00966
7.
Jang
,
J.
,
Lee
,
J.
,
Seol
,
Y. J.
,
Jeong
,
Y. H.
, and
Cho
,
D. W.
,
2013
, “
Improving Mechanical Properties of Alginate Hydrogel by Reinforcement With Ethanol Treated Polycaprolactone Nanofibers
,”
Composites, Part B
,
45
(
1
), pp.
1216
1221
.10.1016/j.compositesb.2012.09.059
8.
Pei
,
B.
,
Wang
,
W.
,
Fan
,
Y.
,
Wang
,
X.
,
Watari
,
F.
, and
Li
,
X.
,
2017
, “
Fiber-Reinforced Scaffolds in Soft Tissue Engineering
,”
Regener. Biomater.
,
4
(
4
), pp.
257
268
.10.1093/rb/rbx021
9.
Eslami
,
M.
,
Vrana
,
N. E.
,
Zorlutuna
,
P.
,
Sant
,
S.
,
Jung
,
S.
,
Masoumi
,
N.
,
Khavari-Nejad
,
R. A.
,
Javadi
,
G.
, and
Khademhosseini
,
A.
,
2014
, “
Fiber-Reinforced Hydrogel Scaffolds for Heart Valve Tissue Engineering
,”
J. Biomater. Appl.
,
29
(
3
), pp.
399
410
.10.1177/0885328214530589
10.
Shafiee
,
A.
, and
Atala
,
A.
,
2017
, “
Tissue Engineering: Toward a New Era of Medicine
,”
Annu. Rev. Med.
,
68
(
1
), pp.
29
40
.10.1146/annurev-med-102715-092331
11.
Xu
,
T.
,
Binder
,
K. W.
,
Albanna
,
M. Z.
,
Dice
,
D.
,
Zhao
,
W.
,
Yoo
,
J. J.
, and
Atala
,
A.
,
2012
, “
Hybrid Printing of Mechanically and Biologically Improved Constructs for Cartilage Tissue Engineering Applications
,”
Biofabrication
,
5
(
1
), p.
015001
.10.1088/1758-5082/5/1/015001
12.
Jang
,
J.
,
Oh
,
H.
,
Lee
,
J.
,
Song
,
T. H.
,
Hun Jeong
,
Y.
, and
Cho
,
D. W.
,
2013
, “
A Cell-Laden Nanofiber/Hydrogel Composite Structure With Tough-Soft Mechanical Property
,”
Appl. Phys. Lett.
,
102
(
21
), p.
211914
.10.1063/1.4808082
13.
Erndt-Marino
,
J. D.
,
Becerra-Bayona
,
S.
,
McMahon
,
R. E.
,
Goldstein
,
A. S.
, and
Hahn
,
M. S.
,
2016
, “
Cell Layer-Electrospun Mesh Composites for Coronary Artery Bypass Grafts
,”
J. Biomed. Mater. Res., Part A
,
104
(
9
), pp.
2200
2209
.10.1002/jbm.a.35753
14.
McMahon
,
R. E.
,
Qu
,
X.
,
Jimenez-Vergara
,
A. C.
,
Bashur
,
C. A.
,
Guelcher
,
S. A.
,
Goldstein
,
A. S.
, and
Hahn
,
M. S.
,
2011
, “
Hydrogel–Electrospun Mesh Composites for Coronary Artery Bypass Grafts
,”
Tissue Eng., Part C
,
17
(
4
), pp.
451
461
.10.1089/ten.tec.2010.0427
15.
Ahn
,
H.
,
Ju
,
Y. M.
,
Takahashi
,
H.
,
Williams
,
D. F.
,
Yoo
,
J. J.
,
Lee
,
S. J.
,
Okano
,
T.
, and
Atala
,
A.
,
2015
, “
Engineered Small Diameter Vascular Grafts by Combining Cell Sheet Engineering and Electrospinning Technology
,”
Acta Biomater.
,
16
, pp.
14
22
.10.1016/j.actbio.2015.01.030
16.
Ju
,
Y. M.
,
Choi
,
J. S.
,
Atala
,
A.
,
Yoo
,
J. J.
, and
Lee
,
S. J.
,
2010
, “
Bilayered Scaffold for Engineering Cellularized Blood Vessels
,”
Biomaterials
,
31
(
15
), pp.
4313
4321
.10.1016/j.biomaterials.2010.02.002
17.
Chronakis
,
I. S.
,
2005
, “
Novel Nanocomposites and Nanoceramics Based on Polymer Nanofibers Using Electrospinning Process—A Review
,”
J. Mater. Process. Technol.
,
167
(
2–3
), pp.
283
293
.10.1016/j.jmatprotec.2005.06.053
18.
Sill
,
T. J.
, and
von Recum
,
H. A.
,
2008
, “
Electrospinning: Applications in Drug Delivery and Tissue Engineering
,”
Biomaterials
,
29
(
13
), pp.
1989
2006
.10.1016/j.biomaterials.2008.01.011
19.
Schiffman
,
J. D.
, and
Schauer
,
C. L.
,
2008
, “
A Review: Electrospinning of Biopolymer Nanofibers and Their Applications
,”
Polym. Rev.
,
48
(
2
), pp.
317
352
.10.1080/15583720802022182
20.
Collins
,
G.
,
Federici
,
J.
,
Imura
,
Y.
, and
Catalani
,
L. H.
,
2012
, “
Charge Generation, Charge Transport, and Residual Charge in the Electrospinning of Polymers: A Review of Issues and Complications
,”
J. Appl. Phys.
,
111
(
4
), p.
044701
.10.1063/1.3682464
21.
Lee
,
J.
,
Jeong
,
Y. H.
, and
Cho
,
D. W.
,
2014
, “
Fabrication of Nanofibrous Mats With Uniform Thickness and Fiber Density
,”
Macromol. Mater. Eng.
,
299
(
9
), pp.
1052
1061
.10.1002/mame.201300390
22.
Nowak
,
J. F.
,
Clippinger
,
A.
, and
Samuel
,
J.
,
2020
, “
Freeform Fabrication of Fiber-Reinforced Hydrogels Using Direct-Write Far-Field Electrospinning
,”
J. Manuf. Process
,
58
, pp.
955
963
.10.1016/j.jmapro.2020.08.041
23.
Zhang
,
S.
,
Campagne
,
C.
, and
Salaün
,
F.
,
2019
, “
Preparation of Electrosprayed Poly(Caprolactone) Microparticles Based on Green Solvents and Related Investigations on the Effects of Solution Properties as Well as Operating Parameters
,”
Coatings
,
9
(
2
), p.
84
.10.3390/coatings9020084
24.
He
,
Y.
,
Yang
,
F.
,
Zhao
,
H.
,
Gao
,
Q.
,
Xia
,
B.
, and
Fu
,
J.
,
2016
, “
Research on the Printability of Hydrogels in 3D Bioprinting
,”
Sci. Rep.
,
6
(
13
), p.
29977
.10.1038/srep29977
25.
Xu
,
S.
,
Deng
,
L.
,
Zhang
,
J.
,
Yin
,
L.
, and
Dong
,
A.
,
2016
, “
Composites of Electrospun-Fibers and Hydrogels: A Potential Solution to Current Challenges in Biological and Biomedical Field
,”
J. Biomed. Mater. Res., Part B
,
104
(
3
), pp.
640
656
.10.1002/jbm.b.33420
26.
Drury
,
J. L.
,
Dennis
,
R. G.
, and
Mooney
,
D. J.
,
2004
, “
The Tensile Properties of Alginate Hydrogels
,”
Biomaterials
,
25
(
16
), pp.
3187
3199
.10.1016/j.biomaterials.2003.10.002
27.
Gauvin
,
R.
,
Guillemette
,
M.
,
Galbraith
,
T.
,
Bourget
,
J.-M.
,
Larouche
,
D.
,
Marcoux
,
H.
,
Aubé
,
D.
,
Hayward
,
C.
,
Auger
,
F. A.
, and
Germain
,
L.
,
2011
, “
Mechanical Properties of Tissue-Engineered Vascular Constructs Produced Using Arterial or Venous Cells
,”
Tissue Eng., Part A
,
17
(
15–16
), pp.
2049
2059
.10.1089/ten.tea.2010.0613
28.
Vande Geest
,
J. P.
,
Dillavou
,
E. D.
,
Di Martino
,
E. S.
,
Oberdier
,
M.
,
Bohra
,
A.
,
Makaroun
,
M. S.
, and
Vorp
,
D. A.
,
2006
, “
Gender-Related Differences in the Tensile Strength of Abdominal Aortic Aneurysm
,”
Ann. N. Y. Acad. Sci.
,
1085
(
1
), pp.
400
402
.10.1196/annals.1383.048
29.
Pichamuthu
,
J. E.
,
Phillippi
,
J. A.
,
Cleary
,
D. A.
,
Chew
,
D. W.
,
Hempel
,
J.
,
Vorp
,
D. A.
, and
Gleason
,
T. G.
,
2013
, “
Differential Tensile Strength and Collagen Composition in Asecending Aortic Aneurysms by Aortic Valve Phenotype
,”
Ann. Thorac. Surg.
,
96
(
6
), pp.
2147
2154
.10.1016/j.athoracsur.2013.07.001
30.
Lang
,
R. M.
,
Cholley
,
B. P.
,
Korcarz
,
C.
,
Marcus
,
R. H.
, and
Shroff
,
S. G.
,
1994
, “
Measurement of Regional Elastic Properties of the Human Aorta: A New Application of Transesophageal Echocardiography With Automated Border Detection and Calibrated Subclavian Pulse Tracings
,”
Circulation
,
90
(
4
), pp.
1875
1882
.10.1161/01.CIR.90.4.1875
31.
Ebrahimi
,
A. P.
,
2009
, “
Mechanical Properties of Normal and Diseased Cerebrovascular System
,”
J. Vasc. Interv. Neurol.
,
2
(
2
), pp.
155
162
.https://pubmed.ncbi.nlm.nih.gov/22518247/
32.
Plott
,
J.
, and
Shih
,
A.
,
2017
, “
The Extrusion-Based Additive Manufacturing of Moisture-Cured Silicone Elastomer With Minimal Void for Pneumatic Actuators
,”
Addit. Manuf.
,
17
, pp.
1
14
.10.1016/j.addma.2017.06.009
33.
Morejon
,
A.
,
Norberg
,
C. D.
,
De Rosa
,
M.
,
Best
,
T. M.
,
Jackson
,
A. R.
, and
Travascio
,
F.
,
2021
, “
Compressive Properties and Hydraulic Permeability of Human Meniscus: Relationships With Tissue Structure and Composition
,”
Front. Bioeng. Biotechnol.
,
8
, p.
622552
.10.3389/fbioe.2020.622552
You do not currently have access to this content.